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MAPKs Influence Pollen Tube Growth by Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain.
Plant Cell. 2017 12; 29(12):3030-3050.PC

Abstract

An apical plasma membrane domain enriched in the regulatory phospholipid phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2] is critical for polar tip growth of pollen tubes. How the biosynthesis of PtdIns(4,5)P2 by phosphatidylinositol 4-phosphate 5-kinases (PI4P 5-kinases) is controlled by upstream signaling is currently unknown. The pollen-expressed PI4P 5-kinase PIP5K6 is required for clathrin-mediated endocytosis and polar tip growth in pollen tubes. Here, we identify PIP5K6 as a target of the pollen-expressed mitogen-activated protein kinase MPK6 and characterize the regulatory effects. Based on an untargeted mass spectrometry approach, phosphorylation of purified recombinant PIP5K6 by pollen tube extracts could be attributed to MPK6. Recombinant MPK6 phosphorylated residues T590 and T597 in the variable insert of the catalytic domain of PIP5K6, and this modification inhibited PIP5K6 activity in vitro. PIP5K6 interacted with MPK6 in yeast two-hybrid tests, immuno-pull-down assays, and by bimolecular fluorescence complementation at the apical plasma membrane of pollen tubes. In vivo, MPK6 expression resulted in reduced plasma membrane association of a fluorescent PtdIns(4,5)P2 reporter and decreased endocytosis without impairing membrane association of PIP5K6. Effects of PIP5K6 expression on pollen tube growth and cell morphology were attenuated by coexpression of MPK6 in a phosphosite-dependent manner. Our data indicate that MPK6 controls PtdIns(4,5)P2 production and membrane trafficking in pollen tubes, possibly contributing to directional growth.

Authors+Show Affiliations

Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Microbial Biotechnology, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Plant Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Plant Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Plant Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany.Department of Stress and Developmental Biology, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany.Proteome Analytics, Leibniz Institute of Plant Biochemistry, 06120 Halle (Saale), Germany.Department of Cellular Biochemistry, Institute of Biochemistry and Biotechnology, Martin-Luther-University Halle-Wittenberg, 06120 Halle (Saale), Germany ingo.heilmann@biochemtech.uni-halle.de.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29167320

Citation

Hempel, Franziska, et al. "MAPKs Influence Pollen Tube Growth By Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain." The Plant Cell, vol. 29, no. 12, 2017, pp. 3030-3050.
Hempel F, Stenzel I, Heilmann M, et al. MAPKs Influence Pollen Tube Growth by Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain. Plant Cell. 2017;29(12):3030-3050.
Hempel, F., Stenzel, I., Heilmann, M., Krishnamoorthy, P., Menzel, W., Golbik, R., Helm, S., Dobritzsch, D., Baginsky, S., Lee, J., Hoehenwarter, W., & Heilmann, I. (2017). MAPKs Influence Pollen Tube Growth by Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain. The Plant Cell, 29(12), 3030-3050. https://doi.org/10.1105/tpc.17.00543
Hempel F, et al. MAPKs Influence Pollen Tube Growth By Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain. Plant Cell. 2017;29(12):3030-3050. PubMed PMID: 29167320.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - MAPKs Influence Pollen Tube Growth by Controlling the Formation of Phosphatidylinositol 4,5-Bisphosphate in an Apical Plasma Membrane Domain. AU - Hempel,Franziska, AU - Stenzel,Irene, AU - Heilmann,Mareike, AU - Krishnamoorthy,Praveen, AU - Menzel,Wilhelm, AU - Golbik,Ralph, AU - Helm,Stefan, AU - Dobritzsch,Dirk, AU - Baginsky,Sacha, AU - Lee,Justin, AU - Hoehenwarter,Wolfgang, AU - Heilmann,Ingo, Y1 - 2017/11/22/ PY - 2017/07/12/received PY - 2017/10/12/revised PY - 2017/11/18/accepted PY - 2017/11/24/pubmed PY - 2019/4/24/medline PY - 2017/11/24/entrez SP - 3030 EP - 3050 JF - The Plant cell JO - Plant Cell VL - 29 IS - 12 N2 - An apical plasma membrane domain enriched in the regulatory phospholipid phosphatidylinositol 4,5-bisphosphate [PtdIns(4,5)P2] is critical for polar tip growth of pollen tubes. How the biosynthesis of PtdIns(4,5)P2 by phosphatidylinositol 4-phosphate 5-kinases (PI4P 5-kinases) is controlled by upstream signaling is currently unknown. The pollen-expressed PI4P 5-kinase PIP5K6 is required for clathrin-mediated endocytosis and polar tip growth in pollen tubes. Here, we identify PIP5K6 as a target of the pollen-expressed mitogen-activated protein kinase MPK6 and characterize the regulatory effects. Based on an untargeted mass spectrometry approach, phosphorylation of purified recombinant PIP5K6 by pollen tube extracts could be attributed to MPK6. Recombinant MPK6 phosphorylated residues T590 and T597 in the variable insert of the catalytic domain of PIP5K6, and this modification inhibited PIP5K6 activity in vitro. PIP5K6 interacted with MPK6 in yeast two-hybrid tests, immuno-pull-down assays, and by bimolecular fluorescence complementation at the apical plasma membrane of pollen tubes. In vivo, MPK6 expression resulted in reduced plasma membrane association of a fluorescent PtdIns(4,5)P2 reporter and decreased endocytosis without impairing membrane association of PIP5K6. Effects of PIP5K6 expression on pollen tube growth and cell morphology were attenuated by coexpression of MPK6 in a phosphosite-dependent manner. Our data indicate that MPK6 controls PtdIns(4,5)P2 production and membrane trafficking in pollen tubes, possibly contributing to directional growth. SN - 1532-298X UR - https://www.unboundmedicine.com/medline/citation/29167320/MAPKs_Influence_Pollen_Tube_Growth_by_Controlling_the_Formation_of_Phosphatidylinositol_45_Bisphosphate_in_an_Apical_Plasma_Membrane_Domain_ L2 - http://www.plantcell.org/cgi/pmidlookup?view=long&pmid=29167320 DB - PRIME DP - Unbound Medicine ER -